Top

Published in:

01-09-2018 | Short Communication

Brain structure mediates the association between height and cognitive ability

Authors: Eero Vuoksimaa, Matthew S. Panizzon, Carol E. Franz, Christine Fennema-Notestine, Donald J. Hagler Jr., Michael J. Lyons, Anders M. Dale, William S. Kremen

Published in: Brain Structure and Function | Issue 7/2018

Abstract

Height and general cognitive ability are positively associated, but the underlying mechanisms of this relationship are not well understood. Both height and general cognitive ability are positively associated with brain size. Still, the neural substrate of the height-cognitive ability association is unclear. We used a sample of 515 middle-aged male twins with structural magnetic resonance imaging data to investigate whether the association between height and cognitive ability is mediated by cortical size. In addition to cortical volume, we used genetically, ontogenetically and phylogenetically distinct cortical metrics of total cortical surface area and mean cortical thickness. Height was positively associated with general cognitive ability and total cortical volume and cortical surface area, but not with mean cortical thickness. Mediation models indicated that the well-replicated height-general cognitive ability association is accounted for by individual differences in total cortical volume and cortical surface area (highly heritable metrics related to global brain size), and that the genetic association between cortical surface area and general cognitive ability underlies the phenotypic height-general cognitive ability relationship.

Available only for authorised users

Adair LS, Fall CH, Osmond C, Stein AD, Martorell R, Ramirez-Zea M, Sachdev HS, Dahly DL, Bas I, Norris SA et al (2013) Associations of linear growth and relative weight gain during early life with adult health and human capital in countries of low and middle income: findings from five birth cohort studies. Lancet 382:525–534. https://doi.org/10.1016/S0140-6736(13)60103-8 CrossRefPubMedPubMedCentral

Adams HH, Hibar DP, Chouraki V, Stein JL, Nyquist PA, Renteria ME, Trompet S, Arias-Vasquez A, Seshadri S, Desrivieres S et al (2016) Novel genetic loci underlying human intracranial volume identified through genome-wide association. Nat Neurosci 19:1569–1582. https://doi.org/10.1038/nn.4398 CrossRefPubMedPubMedCentral

Andreasen NC, Flaum M, Swayze V 2nd, O’Leary DS, Alliger R, Cohen G, Ehrhardt J, Yuh WT (1993) Intelligence and brain structure in normal individuals. Am J Psychiatry 150:130–134. https://doi.org/10.1176/ajp.150.1.130 CrossRefPubMed

Brouwer RM, van Soelen IL, Swagerman SC, Schnack HG, Ehli EA, Kahn RS, Hulshoff Pol HE, Boomsma DI (2014) Genetic associations between intelligence and cortical thickness emerge at the start of puberty. Hum Brain Mapp 35:3760–3773. https://doi.org/10.1002/hbm.22435 CrossRefPubMed

Butler AA, Le Roith D (2001) Control of growth by the somatropic axis: growth hormone and the insulin-like growth factors have related and independent roles. Annu Rev Physiol 63:141–164. https://doi.org/10.1146/annurev.physiol.63.1.141 CrossRefPubMed

Cox SR, Bastin ME, Ritchie SJ, Dickie DA, Liewald DC, Munoz Maniega S, Redmond P, Royle NA, Pattie A, Valdes Hernandez M et al (2018) Brain cortical characteristics of lifetime cognitive ageing. Brain Struct Funct 223:509–518. https://doi.org/10.1007/s00429-017-1505-0 CrossRefPubMed

D’Ercole AJ, Ye P, Calikoglu AS, Gutierrez-Ospina G (1996) The role of the insulin-like growth factors in the central nervous system. Mol Neurobiol 13:227–255. https://doi.org/10.1007/BF02740625 CrossRefPubMed

Dale AM, Sereno MI (1993) Improved localizadon of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach. J Cogn Neurosci 5:162–176. https://doi.org/10.1162/jocn.1993.5.2.162 CrossRefPubMed

Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:179–194. https://doi.org/10.1006/nimg.1998.0395 CrossRefPubMed

Ducharme S, Albaugh MD, Nguyen TV, Hudziak JJ, Mateos-Perez JM, Labbe A, Evans AC, Karama S, Brain Development Cooperative Group (2016) Trajectories of cortical thickness maturation in normal brain development—the importance of quality control procedures. Neuroimage 125:267–279. https://doi.org/10.1016/j.neuroimage.2015.10.010 CrossRefPubMed

Eyler LT, Chen CH, Panizzon MS, Fennema-Notestine C, Neale MC, Jak A, Jernigan TL, Fischl B, Franz CE, Lyons MJ et al (2012) A comparison of heritability maps of cortical surface area and thickness and the influence of adjustment for whole brain measures: a magnetic resonance imaging twin study. Twin Res Hum Genet 15:304–314. https://doi.org/10.1017/thg.2012.3 CrossRefPubMedPubMedCentral

Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97:11050–11055. https://doi.org/10.1073/pnas.200033797 CrossRefPubMed

Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage 9:195–207. https://doi.org/10.1006/nimg.1998.0396 CrossRefPubMed

Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S et al (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33:341–355. https://doi.org/10.1016/S0896-6273(02)00569-X CrossRefPubMed

Fischl B, Salat DH, van der Kouwe AJ, Makris N, Segonne F, Quinn BT, Dale AM (2004a) Sequence-independent segmentation of magnetic resonance images. Neuroimage 23 (Suppl 1):S69–S84. https://doi.org/10.1016/j.neuroimage.2004.07.016 CrossRefPubMed

Fischl B, van der Kouwe A, Destrieux C, Halgren E, Segonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D et al (2004b) Automatically parcellating the human cerebral cortex. Cereb Cortex 14:11–22. https://doi.org/10.1093/cercor/bhg087 CrossRefPubMed

Fjell AM, Grydeland H, Krogsrud SK, Amlien I, Rohani DA, Ferschmann L, Storsve AB, Tamnes CK, Sala-Llonch R, Due-Tonnessen P et al (2015) Development and aging of cortical thickness correspond to genetic organization patterns. Proc Natl Acad Sci USA 112:15462–15467. https://doi.org/10.1073/pnas.1508831112 CrossRefPubMed

Forde NJ, Ronan L, Zwiers MP, Schweren LJS, Alexander-Bloch AF, Franke B, Faraone SV, Oosterlaan J, Heslenfeld DJ, Hartman CA et al (2017) Healthy cortical development through adolescence and early adulthood. Brain Struct Funct 222:3653–3663. https://doi.org/10.1007/s00429-017-1424-0 CrossRefPubMedPubMedCentral

Gunnell D, Miller LL, Rogers I, Holly JM, ALSPAC Study Team (2005) Association of insulin-like growth factor I and insulin-like growth factor-binding protein-3 with intelligence quotient among 8- to 9-year-old children in the avon longitudinal study of parents and children. Pediatrics 116:e681–e686CrossRef

Harris MA, Brett CE, Deary IJ, Starr JM (2016) Associations among height, body mass index and intelligence from age 11 to age 78 years. BMC Geriatr 16:167. https://doi.org/10.1186/s12877-016-0340-0 CrossRefPubMedPubMedCentral

Humphreys LG, Davey TC, Park RK (1985) Longitudinal correlation analysis of standing height and intelligence. Child Dev 56:1465–1478CrossRef

Keller MC, Garver-Apgar CE, Wright MJ, Martin NG, Corley RP, Stallings MC, Hewitt JK, Zietsch BP (2013) The genetic correlation between height and IQ: shared genes or assortative mating? PLoS Genet 9:e1003451. https://doi.org/10.1371/journal.pgen.1003451 CrossRefPubMedPubMedCentral

Kremen WS, Thompson-Brenner H, Leung YM, Grant MD, Franz CE, Eisen SA, Jacobson KC, Boake C, Lyons MJ (2006) Genes, environment, and time: the Vietnam Era Twin Study of Aging (VETSA). Twin Res Hum Genet 9:1009–1022. https://doi.org/10.1375/183242706779462750 CrossRefPubMed

Kremen WS, Prom-Wormley E, Panizzon MS, Eyler LT, Fischl B, Neale MC, Franz CE, Lyons MJ, Pacheco J, Perry ME et al (2010) Genetic and environmental influences on the size of specific brain regions in midlife: the VETSA MRI study. Neuroimage 49:1213–1223. https://doi.org/10.1016/j.neuroimage.2009.09.043 CrossRefPubMed

Kremen WS, Franz CE, Lyons MJ (2013) VETSA: the Vietnam Era Twin Study of Aging. Twin Res Hum Genet 16:399–402. https://doi.org/10.1017/thg.2012.86 CrossRefPubMed

Li G, Nie J, Wang L, Shi F, Lin W, Gilmore JH, Shen D (2013) Mapping region-specific longitudinal cortical surface expansion from birth to 2 years of age. Cereb Cortex 23:2724–2733. https://doi.org/10.1093/cercor/bhs265 CrossRefPubMed

Lundgren EM, Cnattingius S, Jonsson B, Tuvemo T (2001) Intellectual and psychological performance in males born small for gestational age with and without catch-up growth. Pediatr Res 50:91–96. https://doi.org/10.1203/00006450-200107000-00017 CrossRefPubMed

Lundgren EM, Tuvemo T, Gustafsson J (2011) Short adult stature and overweight are associated with poor intellectual performance in subjects born preterm. Horm Res Paediatr 75:138–145. https://doi.org/10.1159/000322015 CrossRefPubMed

Lyall AE, Shi F, Geng X, Woolson S, Li G, Wang L, Hamer RM, Shen D, Gilmore JH (2015) Dynamic development of regional cortical thickness and surface area in early childhood. Cereb Cortex 25:2204–2212. https://doi.org/10.1093/cercor/bhu027 CrossRefPubMed

Lyons MJ, York TP, Franz CE, Grant MD, Eaves LJ, Jacobson KC, Schaie KW, Panizzon MS, Boake C, Xian H et al (2009) Genes determine stability and the environment determines change in cognitive ability during 35 years of adulthood. Psychol Sci 20:1146–1152. https://doi.org/10.1111/j.1467-9280.2009.02425.x CrossRefPubMedPubMedCentral

Lyons MJ, Panizzon MS, Liu W, McKenzie R, Bluestone NJ, Grant MD, Franz CE, Vuoksimaa EP, Toomey R, Jacobson KC et al (2017) A longitudinal twin study of general cognitive ability over four decades. Dev Psychol 53:1170–1177. https://doi.org/10.1037/dev0000303 CrossRefPubMedPubMedCentral

Marioni RE, Batty GD, Hayward C, Kerr SM, Campbell A, Hocking LJ, Generation Scotland, Porteous DJ, Visscher PM, Deary IJ (2014) Common genetic variants explain the majority of the correlation between height and intelligence: the generation Scotland study. Behav Genet 44:91–96. https://doi.org/10.1007/s10519-014-9644-z CrossRefPubMedPubMedCentral

Narducci R, Baroncelli L, Sansevero G, Begenisic T, Prontera C, Sale A, Cenni MC, Berardi N, Maffei L (2018) Early impoverished environment delays the maturation of cerebral cortex. Sci Rep 8:1187. https://doi.org/10.1038/s41598-018-19459-y CrossRefPubMedPubMedCentral

NCD Risk Factor Collaboration (NCD-RisC) (2016) A century of trends in adult human height. Elife. https://doi.org/10.7554/eLife.13410 CrossRef

Neale MC, Cardon LR (1992) Methodology for genetic studies of twins and families. Kluwer, DordrechtCrossRef

Panizzon MS, Fennema-Notestine C, Eyler LT, Jernigan TL, Prom-Wormley E, Neale M, Jacobson K, Lyons MJ, Grant MD, Franz CE et al (2009) Distinct genetic influences on cortical surface area and cortical thickness. Cereb Cortex 19:2728–2735. https://doi.org/10.1093/cercor/bhp026 CrossRefPubMedPubMedCentral

Pietschnig J, Penke L, Wicherts JM, Zeiler M, Voracek M (2015) Meta-analysis of associations between human brain volume and intelligence differences: how strong are they and what do they mean? Neurosci Biobehav Rev 57:411–432. https://doi.org/10.1016/j.neubiorev.2015.09.017 CrossRefPubMed

Posthuma D, de Geus EJ, Neale MC, Hulshoff Pol HE, Baare WEC, Kahn RS, Boomsma D (2000) Multivariate genetic analysis of brain structure in an extended twin design. Behav Genet 30:311–319CrossRef

Posthuma D, De Geus EJ, Baare WF, Hulshoff Pol HE, Kahn RS, Boomsma DI (2002) The association between brain volume and intelligence is of genetic origin. Nat Neurosci 5:83–84. https://doi.org/10.1038/nn0202-83 CrossRefPubMed

Raznahan A, Greenstein D, Lee NR, Clasen LS, Giedd JN (2012) Prenatal growth in humans and postnatal brain maturation into late adolescence. Proc Natl Acad Sci USA 109:11366–11371. https://doi.org/10.1073/pnas.1203350109 CrossRefPubMed

Remer J, Croteau-Chonka E, Dean DC 3rd, D’Arpino S, Dirks H, Whiley D, Deoni SCL (2017) Quantifying cortical development in typically developing toddlers and young children, 1–6 years of age. Neuroimage 153:246–261. https://doi.org/10.1016/j.neuroimage.2017.04.010 CrossRefPubMedPubMedCentral

Ritchie SJ, Dickie DA, Cox SR, Valdes Hernandez MDC, Sibbett R, Pattie A, Anblagan D, Redmond P, Royle NA, Corley J et al (2018) Brain structural differences between 73- and 92-year olds matched for childhood intelligence, social background, and intracranial volume. Neurobiol Aging 62:146–158. https://doi.org/10.1016/j.neurobiolaging.2017.10.005 CrossRefPubMedPubMedCentral

Russ TC, Kivimaki M, Starr JM, Stamatakis E, Batty GD (2014) Height in relation to dementia death: individual participant meta-analysis of 18 UK prospective cohort studies. Br J Psychiatry 205:348–354. https://doi.org/10.1192/bjp.bp.113.142984 CrossRefPubMedPubMedCentral

Sammallahti S, Pyhala R, Lahti M, Lahti J, Pesonen AK, Heinonen K, Hovi P, Eriksson JG, Strang-Karlsson S, Andersson S et al (2014) Infant growth after preterm birth and neurocognitive abilities in young adulthood. J Pediatr 165:1109–1115.e3. https://doi.org/10.1016/j.jpeds.2014.08.028 CrossRefPubMed

Silventoinen K, Posthuma D, van Beijsterveldt T, Bartels M, Boomsma DI (2006) Genetic contributions to the association between height and intelligence: evidence from Dutch twin data from childhood to middle age. Genes Brain Behav 5:585–595. https://doi.org/10.1111/j.1601-183X.2006.00208.x CrossRefPubMed

Silventoinen K, Iacono WG, Krueger R, McGue M (2012) Genetic and environmental contributions to the association between anthropometric measures and IQ: a study of Minnesota twins at age 11 and 17. Behav Genet 42:393–401. https://doi.org/10.1007/s10519-011-9521-y CrossRefPubMed

Solsnes AE, Grunewaldt KH, Bjuland KJ, Stavnes EM, Bastholm IA, Aanes S, Ostgard HF, Haberg A, Lohaugen GC, Skranes J et al (2015) Cortical morphometry and IQ in VLBW children without cerebral palsy born in 2003–2007. Neuroimage Clin 8:193–201. https://doi.org/10.1016/j.nicl.2015.04.004 CrossRefPubMedPubMedCentral

Storsve AB, Fjell AM, Tamnes CK, Westlye LT, Overbye K, Aasland HW, Walhovd KB (2014) Differential longitudinal changes in cortical thickness, surface area and volume across the adult life span: regions of accelerating and decelerating change. J Neurosci 34:8488–8498. https://doi.org/10.1523/JNEUROSCI.0391-14.2014 CrossRefPubMedPubMedCentral

Taki Y, Hashizume H, Sassa Y, Takeuchi H, Asano M, Asano K, Kotozaki Y, Nouchi R, Wu K, Fukuda H et al (2012) Correlation among body height, intelligence, and brain gray matter volume in healthy children. Neuroimage 59:1023–1027. https://doi.org/10.1016/j.neuroimage.2011.08.092 CrossRefPubMed

Tamnes CK, Fjell AM, Ostby Y, Westlye LT, Due-Tonnessen P, Bjornerud A, Walhovd KB (2011) The brain dynamics of intellectual development: waxing and waning white and gray matter. Neuropsychologia 49:3605–3611. https://doi.org/10.1016/j.neuropsychologia.2011.09.012 CrossRefPubMed

Vuoksimaa E, Panizzon MS, Chen CH, Fiecas M, Eyler LT, Fennema-Notestine C, Hagler DJ, Fischl B, Franz CE, Jak A et al (2015) The genetic association between neocortical volume and general cognitive ability is driven by global surface area rather than thickness. Cereb Cortex 25:2127–2137. https://doi.org/10.1093/cercor/bhu018 CrossRefPubMed

Vuoksimaa E, Panizzon MS, Chen CH, Fiecas M, Eyler LT, Fennema-Notestine C, Hagler DJ Jr, Franz CE, Jak AJ, Lyons MJ et al (2016) Is bigger always better? The importance of cortical configuration with respect to cognitive ability. Neuroimage 129:356–366. https://doi.org/10.1016/j.neuroimage.2016.01.049 CrossRefPubMedPubMedCentral

Walhovd KB, Fjell AM, Reinvang I, Lundervold A, Dale AM, Eilertsen DE, Quinn BT, Salat D, Makris N, Fischl B (2005) Effects of age on volumes of cortex, white matter and subcortical structures. Neurobiol Aging 26:1261–1270. https://doi.org/10.1016/j.neurobiolaging.2005.05.020 CrossRefPubMed

Walhovd KB, Krogsrud SK, Amlien IK, Bartsch H, Bjornerud A, Due-Tonnessen P, Grydeland H, Hagler DJ Jr, Haberg AK, Kremen WS et al (2016) Neurodevelopmental origins of lifespan changes in brain and cognition. Proc Natl Acad Sci USA 113:9357–9362. https://doi.org/10.1073/pnas.1524259113 CrossRefPubMed

Walhovd KB, Fjell AM, Giedd J, Dale AM, Brown TT (2017) Through thick and thin: a need to reconcile contradictory results on trajectories in human cortical development. Cereb Cortex 27:1472–1481. https://doi.org/10.1093/cercor/bhv301 CrossRefPubMed

Winkler AM, Kochunov P, Blangero J, Almasy L, Zilles K, Fox PT, Duggirala R, Glahn DC (2010) Cortical thickness or grey matter volume? The importance of selecting the phenotype for imaging genetics studies. Neuroimage 53:1135–1146. https://doi.org/10.1016/j.neuroimage.2009.12.028 CrossRefPubMed

Title: Brain structure mediates the association between height and cognitive ability
Authors: Eero Vuoksimaa
Matthew S. Panizzon
Carol E. Franz
Christine Fennema-Notestine
Donald J. Hagler Jr.
Michael J. Lyons
Anders M. Dale
William S. Kremen
Publication date: 01-09-2018
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 7/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-018-1675-4

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Brain structure mediates the association between height and cognitive ability

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 7/2018

Evidence for a neural dual-process account for adverse effects of cognitive control

Two-photon probes for in vivo multicolor microscopy of the structure and signals of brain cells

The cognitive nuances of surprising events: exposure to unexpected stimuli elicits firing variations in neurons of the dorsal CA1 hippocampus

Decreased hippocampal cell proliferation in mice with experimental antiphospholipid syndrome

GlyT1 determines the glycinergic phenotype of amacrine cells in the mouse retina

Anatomical predictors of cognitive decline after subthalamic stimulation in Parkinson’s disease